Cited by 317Sleep and Wakefulness ResearchCircadian rhythm and melatoninNeuroscience of respiration and sleep

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Identification of preoptic sleep neurons using retrograde labelling and gene profiling

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Chung, Shinjae, Weber, Franz, Zhong, Peng, Tan, Chan Lek, Nguyen, Thuc Nghi, Beier, Kevin T., Hörmann, Nikolai, Chang, Wei-Cheng, Zhang, Zhe, Do, Johnny Phong, Yao, Shenqin, Krashes, Michael J., Tasic, Bosiljka, Cetin, Ali, Zeng, Hongkui, Knight, Zachary A., Luo, Liqun, Dan, Yang·2017·Nature

DOI 10.1038/nature22350PMC PMC5554302

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Abstract

In humans and other mammalian species, lesions in the preoptic area of the hypothalamus cause profound sleep impairment, indicating a crucial role of the preoptic area in sleep generation. However, the underlying circuit mechanism remains poorly understood. Electrophysiological recordings and c-Fos immunohistochemistry have shown the existence of sleep-active neurons in the preoptic area, especially in the ventrolateral preoptic area and median preoptic nucleus. Pharmacogenetic activation of c-Fos-labelled sleep-active neurons has been shown to induce sleep. However, the sleep-active neurons are spatially intermingled with wake-active neurons, making it difficult to target the sleep neurons specifically for circuit analysis. Here we identify a population of preoptic area sleep neurons on the basis of their projection target and discover their molecular markers. Using a lentivirus expressing channelrhodopsin-2 or a light-activated chloride channel for retrograde labelling, bidirectional optogenetic manipulation, and optrode recording, we show that the preoptic area GABAergic neurons projecting to the tuberomammillary nucleus are both sleep active and sleep promoting. Furthermore, translating ribosome affinity purification and single-cell RNA sequencing identify candidate markers for these neurons, and optogenetic and pharmacogenetic manipulations demonstrate that several peptide markers (cholecystokinin, corticotropin-releasing hormone, and tachykinin 1) label sleep-promoting neurons. Together, these findings provide easy genetic access to sleep-promoting preoptic area neurons and a valuable entry point for dissecting the sleep control circuit.

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Authors: Chung, S., Weber, F., Zhong, P., Tan, C. L., Nguyen, T. N., Beier, K. T., Hörmann, N., Chang, W.-C., Zhang, Z., Do, J. P., Yao, S., Krashes, M. J., Tasic, B., Cetin, A., Zeng, H., Knight, Z. A., Luo, L., & Dan, Y.
Affiliations: Howard Hughes Medical Institute (US)
University of California, San Francisco (US)
Allen Institute for Brain Science (US)
National Institutes of Health (US)
Corresponding author: Dan, Yang
ORCID: Chung, Shinjae
Weber, Franz
Zhong, Peng
Tan, Chan Lek
Nguyen, Thuc Nghi
Beier, Kevin T.
Hörmann, Nikolai
Zhang, Zhe
Yao, Shenqin
Krashes, Michael J.
Tasic, Bosiljka
Cetin, Ali
Zeng, Hongkui
Knight, Zachary A.
Luo, Liqun
Dan, Yang
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2017-05
Volume: 545
Issue: 7655
Pages: 477-481
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature22350
PMC: PMC5554302
OpenAlex: W2616271045
Cited by: 317
References: 44
Citations by year: 2026: 25 · 2025: 28 · 2024: 32 · 2023: 28 · 2022: 27 · 2021: 31 · 2020: 26 · 2019: 40 · 2018: 69 · 2017: 10
FWCI: 22.75
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health (1dp2dk109533-01)
National Institute of Mental Health (U01MH105982)
National Institute on Drug Abuse (F32DA038913, K99DA041445)
National Institute of Diabetes and Digestive and Kidney Diseases (DP2-DK109533, R01DK106399)
National Institute of Neurological Disorders and Stroke (R01NS094781)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
Keywords: preoptic area, hypothalamus, sleep regulation, sleep-promoting neurons, GABAergic neurons, tuberomammillary nucleus, retrograde tracing, optogenetics, single-cell RNA sequencing, translating ribosome affinity purification, cholecystokinin, corticotropin-releasing factor
MeSH terms: Channelrhodopsins, Animals, Cholecystokinin, Corticotropin-Releasing Hormone, Female, Hypothalamic Area, Lateral, Male, Neurons, Preoptic Area, Ribosomes, Sleep, Wakefulness, Tachykinins, Biomarkers, Proto-Oncogene Proteins c-fos, Sequence Analysis, RNA, Chloride Channels, Mice, Neuroanatomical Tract-Tracing Techniques, Single-Cell Analysis, GABAergic Neurons, Transcriptome, Optogenetics

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